Olive is a valuable oil-bearing tree with fruits containing high levels of fatty acids. Oil production is a multifaceted process involving intricate interactions between fatty acid biosynthesis and other metabolic pathways that are affected by genetics and the developmental stages of the fruit. However, a comprehensive understanding of the underlying regulatory mechanisms is still lacking. Here, we generated a gap-free telomere-to-telomere assembly for Olea europaea cv. ‘Leccino’, representing an olive genome with the highest contiguity and completeness to date. The combination of time-course metabolomics and transcriptomics datasets revealed a negative correlation between fatty acid and flavonoid biosynthesis in the initial phase of olive fruit development, which was subject to an opposing regulatory mechanism mediated by the hub transcription factor MYC2. Multifaceted molecular assays demonstrated that MYC2 is a repressor of fatty acid biosynthesis by downregulating the expression of BCCP2 (biotin carboxylase carrier protein 2), while it acts as an activator of FLS (flavonol synthase), leading to an increase in flavonoid synthesis. Furthermore, the expression of MYC2 is regulated by fluctuations of methyl jasmonate content during olive fruit development. Our study completes a high-quality gapless genome of an olive cultivar, and provides new insight into the regulatory mechanisms underlying the biosynthesis of fatty acids and flavonoids in its fruit.

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